Sulforaphane inhibits growth of phenotypically different breast cancer cells

Pegram MD, Pauletti G, Slamon DJ (1998) HER-2/neu as a predictive marker of response to breast cancer therapy. Breast Cancer Res Treat 52:65–77

Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL (1987) Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235:177–182

Bianco R, Shin I, Ritter CA, Yakes FM, Basso A, Rosen N, Tsurutani J, Dennis PA, Mills GB, Arteaga CL (2003) Loss of PTEN/MMAC1/TEP in EGF receptor-expressing tumor cells counteracts the antitumor action of EGFR tyrosine kinase inhibitors. Oncogene 22:2812–2822. doi: 10.1038/sj.onc.1206388

Bose S, Crane A, Hibshoosh H, Mansukhani M, Sandweis L, Parsons R (2002) Reduced expression of PTEN correlates with breast cancer progression. Hum Pathol 33:405–409

Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK (2000) Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538–541. doi: 10.1038/35035131

deGraffenried LA, Friedrichs WE, Russell DH, Donzis EJ, Middleton AK, Silva JM, Roth RA, Hidalgo M (2004) Inhibition of mTOR activity restores tamoxifen response in breast cancer cells with aberrant Akt activity. Clin Cancer Res 10:8059–8067. doi: 10.1158/1078-0432.CCR-04-0035

Fahey JW, Zhang Y, Talalay P (1997) Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci USA 94:10367–10372

Zhang Y, Kensler TW, Cho CG, Posner GH, Talalay P (1994) Anticarcinogenic activities of sulforaphane and structurally related synthetic norbornyl isothiocyanates. Proc Natl Acad Sci U S A 91:3147–3150

Singletary K, MacDonald C (2000) Inhibition of benzo[a]pyrene- and 1,6-dinitropyrene-DNA adduct formation in human mammary epithelial cells bydibenzoylmethane and sulforaphane. Cancer Lett 155:47–54

Zhang Y, Talalay P, Cho CG, Posner GH (1992) A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure. Proc Natl Acad Sci U S A 89:2399–2403

Barcelo S, Gardiner JM, Gescher A, Chipman JK (1996) CYP2E1-mediated mechanism of anti-genotoxicity of the broccoli constituent sulforaphane. Carcinogenesis 17:277–282

Gamet-Payrastre L, Li P, Lumeau S, Cassar G, Dupont MA, Chevolleau S, Gasc N, Tulliez J, Terce F (2000) Sulforaphane, a naturally occurring isothiocyanate, induces cell cycle arrest and apoptosis in HT29 human colon cancer cells. Cancer Res 60:1426–1433

Singh SV, Herman-Antosiewicz A, Singh AV, Lew KL, Srivastava SK, Kamath R, Brown KD, Zhang L, Baskaran R (2004) Sulforaphane-induced G2/M phase cell cycle arrest involves checkpoint kinase 2-mediated phosphorylation of cell division cycle 25C. J Biol Chem 279:25813–25822

Singh SV, Srivastava SK, Choi S, Lew KL, Antosiewicz J, Xiao D, Zeng Y, Watkins SC, Johnson CS, Trump DL, Lee YJ, Xiao H, Herman-Antosiewicz A (2005) Sulforaphane-induced cell death in human prostate cancer cells is initiated by reactive oxygen species. J Biol Chem 280:19911–19924. doi: 10.1074/jbc.M412443200

Jackson SJ, Singletary KW (2004) Sulforaphane inhibits human MCF-7 mammary cancer cell mitotic progression and tubulin polymerization. J Nutr 134:2229–2236

Pledgie-Tracy A, Sobolewski MD, Davidson NE (2007) Sulforaphane induces cell type-specific apoptosis in human breast cancer cell lines. Mol Cancer Ther 6:1013–1021

Azarenko O, Okouneva T, Singletary KW, Jordan MA, Wilson L (2008) Suppression of microtubule dynamic instability and turnover in MCF7 breast cancer cells by sulforaphane. Carcinogenesis 29:2360–2368. doi: 10.1093/carcin/bgn241

Xiao D, Powolny AA, Antosiewicz J, Hahm ER, Bommareddy A, Zeng Y, Desai D, Amin S, Herman-Antosiewicz A, Singh SV (2009) Cellular responses to cancer chemopreventive agent D, L-sulforaphane in human prostate cancer cells are initiated by mitochondrial reactive oxygen species. Pharm Res 26:1729–1738

Choi WY, Choi BT, Lee WH, Choi YH (2008) Sulforaphane generates reactive oxygen species leading to mitochondrial perturbation for apoptosis in human leukemia U937 cells. Biomed Pharmacother 62:637–644

Myzak MC, Hardin K, Wang R, Dashwood RH, Ho E (2006) Sulforaphane inhibits histone deacetylase activity in BPH-1, LnCaP and PC-3 prostate epithelial cells. Carcinogenesis 27:811–819. doi: 10.1093/carcin/bgi265

Mi L, Gan N, Cheema A, Dakshanamurthy S, Wang X, Yang DC, Chung FL (2009) Cancer preventive isothiocyanates induce selective degradation of cellular alpha- and beta-tubulins by proteasomes. J Biol Chem 284:17039–17051

Jackson SJ, Singletary KW (2004) Sulforaphane: a naturally occurring mammary carcinoma mitotic inhibitor, which disrupts tubulin polymerization. Carcinogenesis 25:219–227

Konecny GE, Pegram MD, Venkatesan N, Finn R, Yang G, Rahmeh M, Untch M, Rusnak DW, Spehar G, Mullin RJ, Keith BR, Gilmer TM, Berger M, Podratz KC, Slamon DJ (2006) Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer Res 66:1630–1639. doi: 10.1158/0008-5472.CAN-05-1182

Lu Y, Lin YZ, LaPushin R, Cuevas B, Fang X, Yu SX, Davies MA, Khan H, Furui T, Mao M, Zinner R, Hung MC, Steck P, Siminovitch K, Mills GB (1999) The PTEN/MMAC1/TEP tumor suppressor gene decreases cell growth and induces apoptosis and anoikis in breast cancer cells. Oncogene 18:7034–7045. doi: 10.1038/sj.onc.1203183

Yarden RI, Lauber AH, El-Ashry D, Chrysogelos SA (1996) Bimodal regulation of epidermal growth factor receptor by estrogen in breast cancer cells. Endocrinology 137:2739–2747

Watkins SC, Cullen MJ (1987) A qualitative and quantitative study of the ultrastructure of regenerating muscle fibres in Duchenne muscular dystrophy and polymyositis. J Neurol Sci 82:181–192

Herman-Antosiewicz A, Johnson DE, Singh SV (2006) Sulforaphane causes autophagy to inhibit release of cytochrome C and apoptosis in human prostate cancer cells. Cancer Res 66:5828–5835. doi: 10.1158/0008-5472.CAN-06-0139

Levine B, Klionsky DJ (2004) Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 6:463–477

Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC (2002) Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol Cell 10:151–162

Wiczk A, Hofman D, Konopa G, Herman-Antosiewicz A (2012) Sulforaphane, a cruciferous vegetable-derived isothiocyanate, inhibits protein synthesis in human prostate cancer cells. Biochim Biophys Acta 1823:1295–1305. doi: 10.1016/j.bbamcr.2012.05.020

Kanematsu S, Uehara N, Miki H, Yoshizawa K, Kawanaka A, Yuri T, Tsubura A (2010) Autophagy inhibition enhances sulforaphane-induced apoptosis in human breast cancer cells. Anticancer Res 30:3381–3390

Jo EH, Kim SH, Ahn NS, Park JS, Hwang JW, Lee YS, Kang KS (2007) Efficacy of sulforaphane is mediated by p38 MAP kinase and caspase-7 activations in ER-positive and COX-2-expressed human breast cancer cells. Eur J Cancer Prev 16:505–510. doi: 10.1097/01.cej.0000243856.97479.3b

Telang U, Brazeau DA, Morris ME (2009) Comparison of the effects of phenethyl isothiocyanate and sulforaphane on gene expression in breast cancer and normal mammary epithelial cells. Exp Biol Med (Maywood) 234:287–295. doi: 10.3181/0808-RM-241

Ramirez MC, Singletary K (2009) Regulation of estrogen receptor alpha expression in human breast cancer cells by sulforaphane. J Nutr Biochem 20:195–201. doi: 10.1016/j.jnutbio.2008.02.002

Sakao K, Singh SV (2012) D, L-sulforaphane-induced apoptosis in human breast cancer cells is regulated by the adapter protein p66Shc. J Cell Biochem 113:599–610. doi: 10.1002/jcb.23386

Tseng E, Scott-Ramsay EA, Morris ME (2004) Dietary organic isothiocyanates are cytotoxic in human breast cancer MCF-7 and mammary epithelial MCF-12A cell lines. Exp Biol Med (Maywood) 229:835–842

Meeran SM, Patel SN, Tollefsbol TO (2010) Sulforaphane causes epigenetic repression of hTERT expression in human breast cancer cell lines. PLoS ONE 5:e11457. doi: 10.1371/journal.pone.0011457

Mamane Y, Petroulakis E, LeBacquer O, Sonenberg N (2006) mTOR, translation initiation and cancer. Oncogene 25:6416–6422

Magnuson B, Ekim B, Fingar DC (2012) Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 441:1–21. doi: 10.1042/BJ20110892

Holz MK, Ballif BA, Gygi SP, Blenis J (2005) mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123:569–580

Wang X, Li W, Williams M, Terada N, Alessi DR, Proud CG (2001) Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J 20:4370–4379

Raught B, Peiretti F, Gingras AC, Livingstone M, Shahbazian D, Mayeur GL, Polakiewicz RD, Sonenberg N, Hershey JW (2004) Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J 23:1761–1769

Vaira V, Lee CW, Goel HL, Bosari S, Languino LR, Altieri DC (2007) Regulation of survivin expression by IGF-1/mTOR signaling. Oncogene 26:2678–2684. doi: 10.1038/sj.onc.1210094

Wu GJ, Sinclair CS, Paape J, Ingle JN, Roche PC, James CD, Couch FJ (2000) 17q23 amplifications in breast cancer involve the PAT1, RAD51C, PS6K, and SIGma1B genes. Cancer Res 60:5371–5375

Yamnik RL, Digilova A, Davis DC, Brodt ZN, Murphy CJ, Holz MK (2009) S6 kinase 1 regulates estrogen receptor alpha in control of breast cancer cell proliferation. J Biol Chem 284:6361–6369. doi: 10.1074/jbc.M807532200

Manning BD, Cantley LC (2007) AKT/PKB signaling: navigating downstream. Cell 129:1261–1274. doi: 10.1016/j.cell.2007.06.009

Altomare DA, Testa JR (2005) Perturbations of the AKT signaling pathway in human cancer. Oncogene 24:7455–7464

Shah OJ, Wang Z, Hunter T (2004) Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr Biol 14:1650–1656. doi: 10.1016/j.cub.2004.08.026

Stephens L, Anderson K, Stokoe D, Erdjument-Bromage H, Painter GF, Holmes AB, Gaffney PR, Reese CB, McCormick F, Tempst P, Coadwell J, Hawkins PT (1998) Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science 279:710–714

Yu K, Toral-Barza L, Discafani C, Zhang WG, Skotnicki J, Frost P, Gibbons JJ (2001) mTOR, a novel target in breast cancer: the effect of CCI-779, an mTOR inhibitor, in preclinical models of breast cancer. Endocr Relat Cancer 8:249–258